The most commonly reported mechanism of tolerance to piercing-sucking insects has involved photosynthetic activity. Numerous studies have documented general reductions in total chlorophyll and carotenoids in susceptible plants in response to hemipteran feeding. Heng-Moss et al. (2003b) reported reductions of chlorophyll a and b and carotenoid concentrations on susceptible wheat lines in response to Diuraphis noxia (Russian wheat aphid) feeding, suggesting that D. noxia feeding possibly damages the light harvesting complex II, where chlorophylls a and b and carotenoids are important chromophores. Conversely, chlorophyll concentrations were similar between infested plants and their uninfested counterparts in the aphid-resistant isolines, suggesting that aphid feeding may have less effect on chlorophyll loss in D. noxia resistant wheat lines (Heng-Moss et al., 2003b). Botha et al. (2006) similarly reported a significant decrease of total chlorophyll in a susceptible wheat line when fed upon by D. noxia, compared to the resistant wheat. Additionally, the resistant wheat line had a significantly higher expression of cpATPase, relative to the susceptible wheat, indicating the potential importance of cpATPase as a compensatory mechanism to D. noxia injury by maintaining photosynthetic activity (Botha et al., 2006). Likewise, increased photosynthetic activity has been corroborated in many examples of tolerance to hemipterans (Burd and Elliott, 1996; Girma et al., 1998; Haile et al., 1999; Botha et al., 2006; Heng-Moss et al., 2006; Franzen et al., 2007; Murugan et al., 2010; Luo et al., 2014; Cao et al., 2015).

Gutsche et al. (2009; barley) and Franzen et al. (2007; wheat) were able to demonstrate that the rate of RuBP regeneration (as estimated from gas exchange measurements) was maintained in aphid-tolerant plants after D. noxia infestation, whereas susceptible plants showed accelerated declines in RuBP regeneration. Heng-Moss et al. (2006) reported photosynthetic mechanisms contributing to tolerance in buffalograss (Buchloë dactyloides) cultivars to the western chinch bug (Blissus occiduus). Notably, after prolonged exposure to chinch bugs, the susceptible buffalograss displayed reductions in photochemical quantum yield and photosynthetic electron transport rate; however, those differences were not observed in the tolerant cultivar (Heng-Moss et al., 2006). Accordingly, the tolerant buffalograss cultivar was able to enhance photosynthesis upon chinch bug attack as a compensatory mechanism to limit injury, while the susceptible cultivar was unable to maintain sufficient photosynthetic rates (Heng-Moss et al., 2006). Similarly, Haile et al. (1999) showed that the chlorophyll fluorescence yield was similar between uninfested and D. noxia infested leaves in a tolerant wheat line. Alternatively, susceptible and resistant (antibiosis) wheat lines, exhibited reduced chlorophyll fluorescence yield and were unable to recover, suggesting that D. noxia injury resulted in a disruption of the electron transport system reducing light absorption for photosynthesis in the susceptible but not the tolerant wheat line (Haile et al., 1999). It is likely that both mechanical (probing; removal of photosynthates) and chemical signals (aphid saliva) could be contributing to these observations.

In response to initial insect feeding, ROS have been recognized as central early signals, integrating environmental information and regulating stress tolerance (Foyer and Noctor, 2005, 2013; Kerchev et al., 2012). Normally, plants display exceptional redox control, using ROS and antioxidants, such as ascorbate and glutathione, to regulate numerous aspects of their biology including metabolism, growth, development and gene expression patterns (Apel and Hirt, 2004; Kotchoni and Gachomo, 2006; Maffei et al., 2007; Wu and Baldwin, 2010; Foyer and Noctor, 2013; Santamaria et al., 2013). Moreover, increasing evidence suggests that ROS signaling is closely related to hormone signaling, with considerable overlap occurring between ROS and the phytohormones, SA and JA pathways (Foyer and Noctor, 2005, 2013; Kwak et al., 2006; Mittler et al., 2011; Kerchev et al., 2012; Santamaria et al., 2013). Under normal conditions, ROS are rapidly detoxified, and cellular redox homeostasis is governed by the presence of enzymes and large pools of antioxidants that remove and buffer against oxidants (Foyer and Noctor, 2005; Foyer et al., 2016). However, an oxidative burst in response to environmental stresses may lead to generation of excessive ROS (Kotchoni and Gachomo, 2006). In this scenario, if the excessive accumulation of ROS is not efficiently removed, it can become toxic to plant cells, rapidly oxidizing and damaging cellular components, and ultimately leading to cell death (Foyer and Noctor, 2005; Kotchoni and Gachomo, 2006). Indeed, both ROS and antioxidants have been strongly implicated in SA signaling, regulation of PCD and the induction of PR proteins associated with systemic acquired resistance (SAR) (Foyer and Noctor, 2005; Foyer et al., 2016).

Based on these findings, a model is suggested (Figure 1) that integrates both the short-term (arbitrarily <5 days) and longer term (>10 days) responses that could underlie the tolerant response. Plants have both constitutive and inducible defenses (Mithöfer and Boland, 2012; Stout, 2013), whose interactions are likely driven by the genotype. Basal immunity (defined here as pre-existing defenses common to genetically related individuals) could be expected to be similar across genotypes within a population of plants with some variations in the strength of this response. ROS-dependent signaling, as a consequence of basal immune response, can be expected to trigger other induced responses with plant hormones as a key hub through which further signals are propagated. However, ROS are signaling molecules as well and can trigger the upregulation of the antioxidant system eventually leading to ROS mitigation. Plant hormones are central to these processes as well. How basal immunity interfaces with genotypic-dependent constitutive responses is less clear (represented with broken black lines ending in arrows in Figure 1). Most frequently, there is considerable overlap between the short-term and 5 to 10 day responses, but they have been separated (as depicted in Figure 1) to indicate that many physiological changes are noticed 5–10 days post infestation. Continued ROS mitigation appears to be a hallmark in tolerant plants, suggesting that mechanisms that permit modulation of cellular redox could be potential pathways for understanding the tolerance response. ROS mitigation appears to be linked to resumption of growth, providing another window to look for genes that both transduce and activate these pathways. It is likely that these changes do not become evident until much later (>10 days) during a plant-hemipteran interaction. Unfortunately, longer-term studies are often confounded by physiological changes that occur as plant mature that can make data interpretation more difficult. Nevertheless, detailed investigations using a range of omics strategies in well-defined tolerance systems are likely to provide significant insights about the traits controlling the tolerance response.

Over the past decade, researchers have evaluated the interrelationships between ROS damage and mitigation arising from quenching failures associated with end-product inhibition of photosynthesis. Several studies have suggested that tolerant plants appear to counteract deleterious effects of ROS accumulation and, consequently, PCD in response to phloem-feeding insects through up-regulation of detoxification mechanisms (Heng-Moss et al., 2004; Franzen et al., 2007; Gutsche et al., 2009; Smith et al., 2010; Ramm et al., 2013, 2015; Sytykiewicz et al., 2014). Sytykiewicz et al. (2014) described a significant increase of superoxide anion radicals (O₂) in maize seedlings infested with Rhopalosiphum padi (Bird cherry-oat aphid). Accordingly, aphid infestation also resulted in a significant increase in transcript abundances of genes encoding GSTs in the resistant maize plants, relative to the susceptible variety, suggesting a potential role of GST in limiting the adverse effects of oxidative stress within the resistant maize (Sytykiewicz et al., 2014). GSTs are central to redox balance in plant cells, and have been implicated in resistance to exogenous stress (Perez and Brown, 2014).

Transcriptional profiling in tolerant and susceptible buffalograsses suggests that a chinch bug tolerant genotype may be physiologically better prepared for chinch bug attack than susceptible plants as a result of relatively high basal levels of POX and POX-1 (peroxidases), CAT (catalase), and GRAS [a gibberellic acid insensitive (GAI), repressor of GAI and scarecrow] transcripts (Ramm et al., 2013). Ramm et al. (2015) further noted that prior to chinch bug feeding the tolerant buffalograss had significantly higher expression of seven POXs, including five GPXs, relative to the susceptible buffalograss. Collectively, this suggest that constitutively elevated levels of ROS scavenging enzymes in tolerant plants may confer the ability to more readily detoxify ROS induced by chinch bug injury without suffering the negative consequences of high cellular levels of ROS. In wheat, transcriptional profiling also revealed that a resistant line, which was better able to tolerate D. noxia injury, had elevated levels of transcripts related to ROS metabolism, including POX and GST, whereas the susceptible line generally showed an increase in AUX related transcripts (Smith et al., 2010).

Taken together, these studies suggest that plant tolerance to hemipterans involves reprogramming of plant physiology and requires some degree of interaction particularly between primary metabolism, photosynthesis and plant defense responses. In cabbage (Brassica oleracea), radish (Raphanus sativus) and Arabidopsis seedlings infested with the green peach aphid (Myzus persicae), there was a differential regulation of nitrogen metabolism in aphid-infested plants relative to uninfested plants. Infestation led to greater enrichment of ¹⁵N in the infested plants, primarily as a result of changes in host N-metabolism. These changes were attributed to increased nitrate reductase activities along with changes in nitrate flux, resulting in greater incorporation of ¹⁵N. When coupled to selective removal of ¹⁴N by aphids, the net result was increasing levels of ¹⁵N in infested plants (Wilson et al., 2011). These data provide more clues into how aphids could modulate plant primary processes, and how tolerant plants might have evolved compensatory mechanisms impacting plant primary metabolism.

Key aspects of cellular changes occurring in a tolerant phenotype are summarized in Figure 2 Perception of hemipteran pests appears to occur within a short time frame <1 h, with some changes observed at an even shorter interval (Santamaria et al., 2013; Tzin et al., 2015). These changes appear to be triggered by a number of cell wall-anchored proteins, including receptors, kinases and RBOHs (Maffei et al., 2007; Louis and Shah, 2013; Hettenhausen et al., 2015; Foyer et al., 2016). Reaction cascades impacted by these proteins include changes in intercellular calcium content and production of superoxide and related ROS. Some of these events are likely part of the innate immunity of plants to pests and/or pathogens (Foyer et al., 2016). Piercing-sucking insects subsequently trigger more specific responses, because the removal of phloem and xylem contents disturbs both the water and nutrient balance in the plant, and effectively modulates chloroplast functions.

Chloroplasts are critical gatekeepers of leaf health, and altering chloroplast physiology has a significant effect on transcription through retrograde signaling and via shifts in the levels of metabolites such as starch, sugars (trehalose), and JA among others (Singh et al., 2011; Schwarzlander et al., 2012; De Clercq et al., 2013). Thus, negative changes in chloroplast metabolism have a larger effect on other leaf functions, including increased production of ROS and overall slower rates of C and N assimilation. In a tolerant phenotype, mechanisms need to be present to minimize damage from increased ROS, support a defense response, while balancing leaf functions to compensate for nutrient removed by pests. Diverting energy to defense can be expected to impact growth, either by depressing growth of existing meristems and/or by reducing the formation of new meristems. In addition, ROS could damage meristematic cells in the shoots or roots directly as well (Figure 2). How these different processes influence each other at a biochemical level is largely unexplored, and deep transcriptional sequencing of multiple tissues in aphid-tolerant plants is absent. Recovery of leaf, meristem and other plant growth functions are the hallmark of a “tolerant phenotype” in the face of manageable pest populations. Recovery of growth requires overcoming the cellular reprogramming caused by hemipteran pests discussed earlier. However, it is not entirely clear if there is successive or simultaneous rebalancing of chloroplast functions, ROS mitigation and increased delivery of nutrients to sinks to promote growth. It is plausible that integration of these processes might be involved in attenuation of the defense response, maintaining higher levels of ROS mitigating systems, compensation of photosynthates lost due to insect herbivory and renewed growth of the meristems (Figure 2). These features appear to be consistent with much of the literature discussed above.